Original Scientific Article Antimicrobial resistance (AMR) is an increasing global concern in small animal veterinary practices. The overuse and misuse of antimicrobials in companion animals can contribute to the spread of AMR between animals and humans. This study aimed to assess small animal veterinarians’ knowledge, attitudes, and behaviors towards antimicrobial use (AMU) and AMR in North Macedonia. A web-based questionnaire was developed, including questions addressing demographics, owner influence on antibiotic prescription and prescribing practices. The response rate of the small animal veterinarians was 47.50% (57/120), with most of them (84.20%) having 1-15 years of work experience. Pearson’s chi-square test of independence was used for contingency tables that met the chi-square assumption, and Fisher’s exact test was conducted for contingency tables that did not. Most veterinarians responded that they had perceived pressure and direct demands from pet owners to prescribe antimicrobials (35.09% frequently, 45.61% occasionally). In the survey, 50.77% of the veterinarians reported frequently administering antibiotics without conducting bacteriological or antimicrobial susceptibility testing. They typically resorted to these tests in cases with recurrent infections, such as skin infections (19.63%), or when empirical therapy is ineffective (14.72%). Based on the findings, it can be concluded that veterinarians play a crucial role in tackling the AMR in North Macedonia. The lack of stewardship programs or guidelines for responsible antimicrobial use in companion animals is a critical issue that requires urgent attention, emphasizing the vital role of veterinarians in combating AMR. https://macvetrev.mk/LoadArticlePdf/361 2024-10-15 103 114 https://doi.org/10.2478/macvetrev-2024-0020 stewardship companion animals guidelines survey awareness Ivana Shikoska false 1 Faculty of Veterinary Medicine-Skopje, Ss. Cyril and Methodius University in Skopje, Lazar Pop Trajkov 5-7, 1000 Skopje, North Macedonia LEAD_AUTHOR Aleksandar Cvetkovikj false 2 Faculty of Veterinary Medicine-Skopje, Ss. Cyril and Methodius University in Skopje, Lazar Pop Trajkov 5-7, 1000 Skopje, North Macedonia AUTHOR Martin Nikolovski false 3 Faculty of Veterinary Medicine-Skopje, Ss. Cyril and Methodius University in Skopje, Lazar Pop Trajkov 5-7, 1000 Skopje, North Macedonia AUTHOR Iskra Cvetkovikj false 4 Faculty of Veterinary Medicine-Skopje, Ss. Cyril and Methodius University in Skopje, Lazar Pop Trajkov 5-7, 1000 Skopje, North Macedonia AUTHOR Marco-Fuertes, A., Marin, C., Lorenzo-Rebenaque, L., Vega, S., Montoro-Dasi, L. (2022). Antimicrobial resistance in companion cnimals: a new challenge for the One Health approach in the European Union. Vet Sci. 9(5): 208. PMid:35622736 PMCid:PMC9146952 1 https://doi.org/10.3390/vetsci9050208 World Health Organization (2021). Global antimicrobial resistance and use surveillance system (GLASS) report: 2021. 2 Joosten, P., Ceccarelli, D., Odent, E., Sarrazin, S., Graveland, H., Van Gompel, L., Battisti, A., et al. (2020). Antimicrobial usage and resistance in companion animals: A cross-sectional study in three european countries. Antibiotics 9(2): 87. PMid:32079072 PMCid:PMC7175148 3 https://doi.org/10.3390/antibiotics9020087 Galarce, N., Arriagada, G., Sánchez, F., Venegas, V., Cornejo, J., Lapierre, L. (2021). Antimicrobial use in companion animals: assessing veterinarians’ prescription patterns through the first national survey in Chile. Animals (Basel). 11(2): 348. PMid:33573203 PMCid:PMC7912091 4 https://doi.org/10.3390/ani11020348 Jin, M., Osman, M., Green, B.A., Yang, Y., Ahuja, A., Lu, Z., Cazer, C.L. (2023). Evidence for the transmission of antimicrobial resistant bacteria between humans and companion animals: a scoping review. One Health 17, 100593. PMid:37448771 PMCid:PMC10336692 5 https://doi.org/10.1016/j.onehlt.2023.100593 Guardabassi, L., Prescott, J.F. (2015). Antimicrobial stewardship in small animal veterinary practice: from theory to practice. Vet Clin North Am Small Anim Pract. 45(2): 361-376. PMid:25721619 6 https://doi.org/10.1016/j.cvsm.2014.11.005 Allerton, F., Prior, C., Bagcigil, A.F., Broens, E., Callens, B., Damborg, P., Dewulf, J., et al. (2021). Overview and evaluation of existing guidelines for rational antimicrobial use in small-animal veterinary practice in europe. Antibiotics 10(4): 409. PMid:33918617 PMCid:PMC8069046 7 https://doi.org/10.3390/antibiotics10040409 Nielsen, S.S., Bicout, D.J., Calistri, P., Canali, E., Drewe, J.A., Garin-Bastuji, B., Gonzales Rojas, J.L., et al. (2021). Assessment of animal diseases caused by bacteria resistant to antimicrobials: dogs and cats. EFSA J. 19(6): e06680. PMid:34194578 PMCid:PMC8237238 8 https://doi.org/10.2903/j.efsa.2021.6680 Lhermie, G., La Ragione, R.M., Weese, J.S., Olsen, J.E., Christensen, J.P., Guardabassi, L. (2020). Indications for the use of highest priority critically important antimicrobials in the veterinary sector. J Antimicrob Chemother. 75(7): 1671-1680. PMid:32240295 9 https://doi.org/10.1093/jac/dkaa104 Pomba, C., Rantala, M., Greko, C., Baptiste, K.E., Catry, B., van Duijkeren, E., Mateus, A., et al. (2017). Public health risk of antimicrobial resistance transfer from companion animals. J Antimicrob Chemother. 72(4): 957-968. PMid:27999066 10 https://doi.org/10.1093/jac/dkw481 Tomanic, D., Stojanovic, D., Belić, B., Davidov, I., Novakov, N., Radinovic, M., Kladar, N., Kovacevic, Z. (2021). Off label use of human approved drugs in treatment of dogs in the Republic of Serbia. Pol J Vet Sci. 24(3): 399-407. PMid:34730304 11 https://doi.org/10.24425/pjvs.2021.138731 European Medicines Agency (EMA). (2017). Sales of veterinary antimicrobial agents in 30 European countries in 2015. Trends from 2010 to 2015. Seventh ESVAC Report. Oj L 135: 1-109. 12 Duarte, A.S.R., Høg, B.B., Korsgaard, H., Attauabi, M., Boel, J., Dalby, T., Hammerum, A.M., et al. (2021). DANMAP 2020 - Use of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, food and humans in Denmark. Statens Serum Institut og Technical University of Denmark. DANMAP. 13 EMA/CVMP/CHMP. (2019). Categorisation of antibiotics in the European Union. Eur Med Agence. 31, 1-73. 14 Frey, E.,Costin, M.,Granick, J., Kornya, M., Weese, J.S. (2022). 2022 AAFP/AAHA antimicrobial stewardship guidelines. J Am Anim Hosp Assoc. 58(4): 1-5. PMid:35793483 15 https://doi.org/10.5326/1547-3317-58.4.1 Mader, R., Muñoz Madero, C., Aasmäe, B., Bourély, C., Broens, E.M., Busani, L., et al. (2022). Review and analysis of national monitoring systems for antimicrobial resistance in animal bacterial pathogens in Europe: A basis for the development of the European antimicrobial resistance surveillance network in veterinary medicine (EARS-Vet). Front Microbiol. 13, 838490. PMid:35464909 PMCid:PMC9023068 16 https://doi.org/10.3389/fmicb.2022.838490 Cvetkovikj, I., Shikoska, I., Ratkova Manovska, M., Prodanov, M., Rashikj, L., Popova, Z., Djadjovski, I., Cvetkovikj, A. (2022). Antimicrobial resistance in Staphylococci isolated from dogs in the Republic of North Macedonia. Days of Vet Med. September, 22-25, (p. 48), Ohrid, North Macedonia. 17 Van Cleven, A., Sarrazin, S., de Rooster, H., Paepe, D., Van der Meeren, S., Dewulf, J. (2018). Antimicrobial prescribing behaviour in dogs and cats by Belgian veterinarians. Vet Rec. 182(11): 324. PMid:29196488 18 https://doi.org/10.1136/vr.104316 Chipangura, J.K., Eagar, H., Kgoete, M., Abernethy, D., Naidoo, V. (2017). An investigation of antimicrobial usage patterns by small animal veterinarians in South Africa. Prev Vet Med. 136, 29-38. PMid:28010905 19 https://doi.org/10.1016/j.prevetmed.2016.11.017 Hopman, N.E.M., Mughini-Gras, L., Speksnijder, D.C., Wagenaar, J.A., van Geijlswijk, I. M., Broens, E.M. (2019). Attitudes and perceptions of Dutch companion animal veterinarians towards antimicrobial use and antimicrobial resistance. Prev Vet Med. 170, 104717. PMid:31421495 20 https://doi.org/10.1016/j.prevetmed.2019.104717 De Briyne, N., Atkinson, J., Pokludová, L., Borriello, S.P., Price, S. (2013). Factors influencing antibiotic prescribing habits and use of sensitivity testing amongst veterinarians in Europe. Vet Rec. 173(19): 475.PMid:24068699 PMCid:PMC3841786 21 https://doi.org/10.1136/vr.101454 Hughes, L.A., Williams, N., Clegg, P., Callaby, R., Nuttall, T., Coyne, K., Pinchbeck, G., Dawson, S. (2012). Cross-sectional survey of antimicrobial prescribing patterns in UK small animal veterinary practice. Prev Vet Med. 104(3-4): 309-316. PMid:22225772 22 https://doi.org/10.1016/j.prevetmed.2011.12.003 Vandeweerd, J.M., Vandeweerd, S., Gustin, C., Keesemaecker, G., Cambier, C., Clegg, P., Saegerman, C., et al. (2012). Understanding veterinary practitioners’ decision-making process: Implications for veterinary medical education. J Vet Med Educ. 39(2): 142-151. PMid:22718001 23 https://doi.org/10.3138/jvme.0911.098R1 Frey, E., Kedrowicz, A., Hedgpeth, M.W. (2024). Decision making on antimicrobial use: cat and dog owners’ knowledge and preferences for veterinary communication. Vet Rec. 194(5): e3411. PMid:37691448 24 https://doi.org/10.1002/vetr.3411 Scarborough, R., Hardefeldt, L., Browning, G., Bailey, K. (2021). Pet owners and antibiotics: knowledge, opinions, expectations, and communication preferences. Antibiotics (Basel). 10(11): 1326. PMid:34827264 PMCid:PMC8615269 25 https://doi.org/10.3390/antibiotics10111326 Jessen, L.R., Damborg, P., Spohr, A. (2019). Antibiotic use guidelines for companion animal practice, 2nd ed. Danish Small Anim Vet Assoc. SvHKS. 26 Timofte, D., Broens, E.M., Guardabassi, L., Pomba, C., Allerton, F., Ikonomopoulos, J., Overesch, G., Damborg, P. (2021). Driving laboratory standardization of bacterial culture and antimicrobial susceptibility testing in veterinary clinical microbiology in Europe and beyond. J Clin Microbiol. 59(6): e02572-20. PMid:33361339 PMCid:PMC8315970 27 https://doi.org/10.1128/JCM.02572-20 Alcantara, G.L.C., Pinello, K.C., Severo, M., Niza-Ribeiro, J. (2021). Antimicrobial resistance in companion animals - Veterinarians’ attitudes and prescription drivers in Portugal. Comp Immunol Microbiol Infect Dis. 76, 101640. PMid:33684640 28 https://doi.org/10.1016/j.cimid.2021.101640 Weese, J.S., Blondeau, J., Boothe, D., Guardabassi, L.G., Gumley, N., Papich, M., Jessen, L.R., et al. (2019). International society for companion animal infectious diseases (ISCAID) guidelines for the diagnosis and management of bacterial urinary tract infections in dogs and cats. Vet J. 247, 8-25. PMid:30971357 29 https://doi.org/10.1016/j.tvjl.2019.02.008 Carmo, L.P., Nielsen, L.R., Alban, L., da Costa, P.M., Schüpbach-Regula, G., Magouras, I. (2018). Veterinary expert opinion on potential drivers and opportunities for changing antimicrobial usage practices in livestock in Denmark, Portugal, and Switzerland. Front Vet Sci. 5, 29. PMid:29546044 PMCid:PMC5837977 30 https://doi.org/10.3389/fvets.2018.00029 Chirollo, C., Nocera, F.P., Piantedosi, D., Fatone, G., Della Valle, G., De Martino, L., Cortese, L. (2021). Data on before and after the traceability system of veterinary antimicrobial prescriptions in small animals at the university veterinary teaching hospital of Naples. Animals 11(3): 913. PMid:33806745 PMCid:PMC8005210 31 https://doi.org/10.3390/ani11030913 Escher, M., Vanni, M., Intorre, L., Caprioli, A., Tognetti, R., Scavia, G. (2011). Use of antimicrobials in companion animal practice: A retrospective study in a veterinary teaching hospital in Italy. J Antimicrob Chemother. 66(4): 920-927. PMid:21393194 32 https://doi.org/10.1093/jac/dkq543 EMA. (2013). Reflection paper on the risk of antimicrobial resistance transfer from companion animals Summary. Ema/Cvmp/Awp/401740/2013. 44, 1-27. 33 Zhuo, A., Labbate, M., Norris, J.M., Gilbert, G.L., Ward, M.P., Bajorek, B.V., Degeling, C., et al. (2018). Opportunities and challenges to improving antibiotic prescribing practices through a One Health approach: results of a comparative survey of doctors, dentists and veterinarians in Australia. BMJ Open 8(3): e020439. PMid:29602857 PMCid:PMC5884343 34 https://doi.org/10.1136/bmjopen-2017-020439 Holloway, S., Trott, D., Shipstone, M., Barrs, V., Malik, R., Burrows, M., Norris, J., et al. (2022). AIDAP Antibiotic prescribing guidelines-companion animals. Aust Infect Dis Advis Painel. 2, 205. 35 Williams, J. (2018). Antimicrobial prophylaxis: the why and how of antimicrobial prophylaxis. BSAVA Companion 11, 4-7. 36 https://doi.org/10.22233/20412495.1118.4 Attauabi, M., Høg, B. B., Müller-Pebody, B. (2021). Summary Danmap 2020: use of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, food and humans in Denmark. Statens Serum Institut og Technical University of Denmark. DANMAP 37 Hillier, A., Lloyd, D.H., Weese, J.S., Blondeau, J.M., Boothe, D., Breitschwerdt, E., Guardabassi, L., et al. (2014). Guidelines for the diagnosis and antimicrobial therapy of canine superficial bacterial folliculitis (antimicrobial guidelines working group of the international society for companion animal infectious diseases). Vet Dermatol. 25(3): 163-e43. 38 Lappin, M.R., Blondeau, J., Boothe, D., Breitschwerdt, E.B., Guardabassi, L., Lloyd, D.H., Papich, M.G., et al. (2017). Antimicrobial use guidelines for treatment of respiratory tract disease in dogs and cats: antimicrobial guidelines working group of the international society for companion animal infectious diseases. J Vet Intern Med. 31(2): 279-294. PMid:28185306 PMCid:PMC5354050 39 https://doi.org/10.1111/jvim.14627 Hur, B.A., Hardefeldt, L.Y., Verspoor, K.M., Baldwin, T., Gilkerson, J.R. (2020). Describing the antimicrobial usage patterns of companion animal veterinary practices; free text analysis of more than 4.4 million consultation records. PLoS One 15(3): e0230049. PMid:32168354 PMCid:PMC7069610 40 https://doi.org/10.1371/journal.pone.0230049 Burke, S., Black, V., Sánchez-Vizcaíno, F., Radford, A., Hibbert, A., Tasker, S. (2017). Use of cefovecin in a UK population of cats attending first-opinion practices as recorded in electronic health records. J Feline Med Surg. 19(6): 687-692. PMid:27507842 PMCid:PMC11128814 41 https://doi.org/10.1177/1098612X16656706 Food and Veterinary Agency of Republic of North Macedonia. (2024). List of veterinary medicinal products that have a marketing authorization, i.e. for which the approval has been cancelled, i.e. for which a change has been made during the validity of the authorization. Official Gazette of Republic of North Macedonia No.111/2024 [in Macedonian]. 42